Growth and physiological responses of Chinese cabbage and radish ...

Hort. Environ. Biotechnol. 52(4):376-386. 2011. DOI 10.1007/s13580-011-0012-0

Research Report

Growth and Physiological Responses of Chinese Cabbage and Radish to Long-term Exposure to Elevated Carbon Dioxide and Temperature 1

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Eun-Young Choi , Tae-Cheol Seo , Sang-Gyu Lee , Il-Hwan Cho , and James Stangoulis

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Department of Horticulture, KonKuk University, Chungju 380-701, Korea Vegetable Research Division, National Institute of Horticultural & Herbal Science, Suwon 440-706, Korea 3 School of Biological Sciences, Flinders University, Sturt Rd, Bedford Park, South Australia 5042, Australia 2

*Corresponding author: [email protected]

Received February 16, 2011 / Accepted June 15, 2011 GKorean Society for Horticultural Science and Springer 2011

Abstract. Future forecasts for climate change predict the global mean surface air temperature rise by 1 - 4Gand double current atmospheric CO2 level before the end of 21 century. Increased atmospheric temperature and CO2 concentration are particularly important concerns for agricultural, horticultural and native plant production. In this study, effects of long-term exposure to elevated temperature and carbon dioxide (CO2) on the growth and physiological responses of 3 cultivars of Chinese radish (Raphanus sativus L.) and 3 cultivars of Chinese cabbage (Brassica campestris L.) were examined. In result, the radishes exposed to elevated CO2 for 90 days after sowing (DAS) resulted in little or no change in the root dry weights and the rate of photosynthesis compared with those grown in ambient levels of CO2. In contrast, long-term exposure to elevated CO2 in cabbage had variable effects on the leaf dry weight. As a result of acclimating to the elevated temperature, the radish ‘Chunha’ had a higher rate of photosynthesis, stomatal conductance and internal CO2 concentration than in the control condition. Furthermore, the long-term exposure to a combination condition of elevated temperature and CO2 increased root dry weights of the radishes ‘Cheongdae’ and ‘Chunha’ more than elevated temperature alone. The combination of elevated CO2 and temperature stimulated the growth of roots more than that of shoots in the radish ‘Chunha’, and thus may have led a higher rate of nutrient uptake than other radish cultivars. In contrast, when the cabbage ‘Chun-gwang’ was exposed to a combination of elevated temperature and CO2 for 90 DAS, the leaf dry weight decreased about 3-fold more than that only exposed to elevated CO2 with drastic decreases in stomatal conductance, internal CO2 and photosynthesis rate. When the cabbage ‘Samjin’ was exposed to either elevated temperature alone or both elevated temperature and CO2 for 80 DAS, the decrease in the leaf dry weight was less than that of the other cabbage cultivars. Results indicated that the radish ‘Chunha’ and the cabbage ‘Samjin’ tolerated either elevated temperature alone or combination condition of elevated temperature and CO2 more than other cultivars. Additional key words: Brassica Campestris L., climate change, nutrient uptake rate, phytotron, Raphanus sativus L.

Lqwurgxfwlrq The global mean surface air temperature is predicted to rise by 1 - 4Gas a result of increased greenhouse gases in the atmosphere by the end of the 21st century (IPCC, 2007). The mean temperature during the year and the winter has risen by 0.7G and 1.4, respectively, since the last 30 years in Korea (Jung et al., 2002). With the increase of atmospheric temperature, an increase in atmospheric CO2 concentration is predicted to nearly double its current level before the end of the 21st century as a result of deforestation and fossil fuel consumption (Morion and lawlor, 1999). Increased temperature and atmospheric CO2 concentration

are particularly important concerns for agricultural, horticultural and native plant production since those parameters have complex effects on plant growth and photosynthetic activity with many factors, such as the efficiency of the carbon fixation pathway (Ceusters et al., 2008). The decrease in photosynthesis at elevated temperature may be due to negative feedback effects from starch and sucrose synthesis that decrease the enzymatic activity of ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco) (Farquhar et al., 1980; Harley and Sharkey, 1991) or alter the physicochemical properties and functional organization of the thylakoid membrane (Berry and Björkman, 1980; Kim and Portis, 2005; Wise et al., 2004). In addition, a few studies have

Hort. Environ. Biotechnol. 52(4):376-386. 2011.

reported that plants grown in the presence of elevated CO2 have higher tolerance to elevated temperatures than those that are grown in normal conditions (Huxman et al., 1998; Taub et al., 2000). However, the effect of the interaction between elevated CO2 and growth temperature on photosynthesis is controversial (Morison and Lawlor, 1999) because the effects of heat stress vary widely in both intensity and duration. Some studies suggested that a combination of elevated CO2 and temperature has positive effects on photosynthesis of certain plant species, including the Mojave Desert evergreen shrub, Larrea tridentata (Hamerlynck et al., 2000) and Cucumis sativus (Taub et al., 2000). For example, when leaves of cucumber grown in normal or elevated CO2 concentration were exposed to temperatures between 28 - 48, those grown in elevated CO2 maintained photosystem II (PSII) efficiency (Fv/Fm) at significantly higher temperatures than those grown in a normal CO2 concentration (Taub et al., 2000). Whereas, the others suggest that it has negative effects on photosynthesis of certain plant species, including Larrea tridentate (Huxman et al., 1998), tree seedlings (Bassow et al., 1994) and eucalyptus species (Roden and Ball, 1996). Most of the published studies on the effect of CO2 and temperature have focused on grasses (Lilly, et al., 2001; Morgan et al., 2001), rice (Ziska et al., 1997), tropical crops (Demmers-Derks et al., 1998; Hogan et al., 1991; Zue et al., 1999), cotton (Reddy et al., 1999), or cereal crops (Alexandrov and Hoogenboom, 2000). However a few studies have examined the interactions of increased CO2 and temperature for vegetable growth and physiological responses, such as cucumber (Taub et al., 2000), soybean (Ziska, 1998) and kidney bean (Vara Prasad et al., 2002). Chinese cabbage and radish, the important cool season crops, are good models to study the effects of climate changes on agricultural production because they are more adversely affected by elevated temperatures than other warm season crops, and greatly influenced by elevated CO2 in terms of change in stomatal resistance (Mishra et al., 1999) and in root to shoot ratio (Idso et al., 1988; Morison and Gifford, 1984). This study examined the effects of elevated CO2 and temperature on the growth, photosynthesis rate, gas exchange, and rate of nutrient uptake in the radishes and cabbages.

Pdwhuldov# dqg# Phwkrgv Sodqw# Jurzwk Chinese radish (Raphanus sativus (L.) ‘Cheongdae’, ‘Chunha’, and ‘Cheong-un’) and Chinese cabbage (Brassica campestris (L.) ‘Chun-gwang’, ‘Jincheong’, and ‘Samjin’) were examined. Seeds of the radishes ‘Cheongdae’ and ‘Chunha’ and the cabbages ‘Chun-gwang’ and ‘Jincheong’, cultivars for spring-summer seasons, were sown on the 12th

377

of May, 2009, while seeds of the radish, ‘Cheong-un’ and the cabbage, ‘Samjin’, cultivars for autumn season, were sown on the 26th of August, 2009. All of the radish cultivars are known to enlarge their roots faster and have denser flesh than other cultivars. The cabbage cultivar, ‘Chun-gwang’, is known to shape proper heading under both low and high temperature. The cabbage cultivar, ‘Jincheong’, is known to have less occurrence and intensity of bolting. The cabbage cultivar, ‘Samjin’ is known to have higher leaf numbers and to have relatively higher resistance to high temperature. The seeds were sown in large plastic pots (400 mm in height and 300 mm in diameter) filled with equivalent of 13 kg of air-dried commercial potting mix with clay soil (8:2 v/v) containing the following nutritional characteristics: Total-N (92 mgkg-1), P2O5 (585 mgkg-1), K (2.3 cmolkg-1), Ca -1 -1 (13 cmolkg ), Mg (2.9 cmolkg ), Organic matter (3.3%), -1 pH (7.4) and EC (4.8 dSm ). Total 24 pots were placed in each of four phytotron glass chambers (2.5 m3) standing outdoors under four separated acrylic plastic roofs at the National Institute of Horticultural and Herbal Science (NIHHS) located in Suwon city. After 8 days after sowing (DAS) in May, 2009, thinning was conducted as intended to leave only vigorous 2 seedlings in each pot. The dry weights of leaves and roots of the thinned seedlings were measured at 8 DAS. Two healthy seedlings of each cultivar of radish or cabbage were then grown in each pot with 6 replications (2 species × 2 cultivars × 6 replications = total 24 pots in each chamber) in the cultivation period between May and August, while total 12 pots were placed in each chamber (2 species × 1 cultivar × 6 replications) in the period between September and November. Four individual plants of the radishes ‘Cheongdae’ and ‘Chunha’ and the cabbages ‘Chun-gwang’ and ‘Jincheong’ were harvested at 20, 45, and 90 DAS for growth measurement, while the radish ‘Cheong-un’, and the cabbage ‘Samjin’, were harvested 25, 60, and 80 DAS. Sodqw# Jurzlqj# Frqglwlrqv Each chamber was assigned one of 2 different CO2 concentrations and 2 different air temperature levels; chamber 1 (ambient temperature + ambient CO2 (fixed as 350 µmol -1 mol )), chamber 2 (ambient temperature + elevated CO2 (fixed as 650 µmolmol-1)), chamber 3 (elevated temperature (ambient + 4) + ambient CO2) and chamber 4 (elevated temperature + elevated CO2). The treatments of fixed CO2 and non-fixed temperature levels were maintained over a 24-h time period during the entire experimental periods. The continuous injection of CO2 was regulated through gas cylinders, which was mixed with ambient air before entering the chamber. Heating air was conducted prior to injection by passing it over a set of heating system. The average maximum and minimum temperatures were 27.5G

378

Eun-Young Choi, Tae-Cheol Seo, Sang-Gyu Lee, Il-Hwan Cho, and James Stangoulis

and 18.3, respectively, between May and August, 2009, while those were 24.4Gand 14.2, respectively, between September and November, 2009. The fixed CO2 level varied about ± 10% from the pre-set CO2 level, and the elevated temperature was maintained within 1.0. A nutrient solution composed of 15N, 3P, 6K, 8Ca, 4Mg meL-1 in pH 6.5 and -2 EC 1.5 dSm was irrigated every 3 days after plants had three leaves. After harvesting and measuring the growth and yield, leaf samples of cabbage and radish were dried at 70G and the root samples of radish were freeze-dried at -70 prior to analysis of tissue concentrations by an Atomic Absorption Spectrometry (AA-6701E, Shimadzu, Japan). Skrwrv|qwkhvlv Photosynthesis rates, stomatal conductance, transpiration rate, internal CO2 concentration and VpdL were measured on fully expanded leaves detached from plant at both 70 and 75 DAS on a clear sunny day between 10:00 and 11:00 h with an open infra-red gas analyzer (model 6400, Li-COR, Lincoln, Nebraska, USA), equipped with a 250 mm3 leaf chamber. Red-blue LED light source (6400-02B Red/Blue LED) were used to give light incidence. Temperature, CO2 concentration and relative humidity conditions in the analyzer were matched to each of the chamber conditions being sampled under 1000 µmolm-2s-1 of photosynthetically active radiation (PAR), which allowed for the determination of CO2 efflux rate in the light (Rl) and the CO2 efflux in the dark, i.e., dark respiration rate (Rd). The CO2 efflux was measured 5 to 10 times at 30-s intervals. Each observation was repeated 4 times on three leaves randomly selected from 3 individual plants of each cultivar.

standard error of the means are presented. Despite the lack of statistical analysis, the similar growth response of plant grown in the separated phytotron chambers suggests that differences between growth rooms are likely to be little and differences between the CO2 and temperature treatments are worth reporting.

Uhvxowv Jurzwk# dqg# \lhog Plant growth and yield varied among the cultivars of radish and cabbage. The root dry weights of the radish cultivars, ‘Cheongdae’ and ‘Chunha,’ grown in elevated CO2 for 45 DAS was higher than that of the same cultivars grown in ambient CO2 conditions (Fig. 1), however at 90

Qxwulhqw# Xswdnh# Udwh -1 The mineral uptake rates per unit of root dry weight (쩋gg -1 root DWday ) were calculated according to Williams (1948). This rate of nutrient uptake was determined only for the radish plant since it is an important indicator for sink capacity of root vegetable. Uptake rate = [(m1-m0)/(DWr1-DWr0)] × [(ln DWr1-ln DW r0)/(t1-t0)] Where m1 and m0 are the total content of each mineral in leaf and root tissues and DW r1 and DW r0 are the root dry weights at day t1 and t0, respectively. Vwdwlvwlfdo# Dqdo|vlv The two different CO2 and two different temperature treatments had to be assigned to four separate phytotron chambers under four separated roofs. Although each chamber is very closely connected in the same place and the external growth condition is similar, the chambers have four separated roofs, which making impossible to perform proper statistical analysis of the data. Therefore, only calculated means and

Fig. 1. Root dry weights of the radishes ‘Cheongdae’ and ‘Chunha’ -1 exposed to either ambient CO2 (350 µmolmol ) or elevated CO2 -1 (650 µmolmol ) in both ambient and elevated temperature (ambient + 4°C) for 45 and 90 DAS and ‘Cheong-un’ for 60 and 80 DAS. Bars represent the mean dry weight for 3 plants ± standard error.


DAS, the root dry weights slightly decreased by 14 ± 0.4% and 30 ± 9.7%, respectively, compared with those grown in ambient levels of CO2. In contrast, elevated CO2 did not have any effect on the dry weight of the roots of the radish ‘Cheong-un’ in either ambient or elevated temperature. The long-term exposure of all 3 radish cultivars to the elevated temperature decreased the dry weight of their roots to different degrees. At 45 DAS, the elevated temperature decreased the root dry weights of the radish ‘Chunha’ and ‘Cheongdae’ by 44 ± 2% and 37 ± 12%, respectively, compared with those that were grown at ambient temperature. However, at 90 DAS, the radish ‘Cheongdae’ had a greatest decrease in root dry weight by 93 ± 1.8%, whereas the decrease for the radish ‘Chunha’ and ‘Cheong-un’ was only 30 ± 8.4% and 26 ± 0.5%, respectively. Furthermore, the long-term exposure to a combination of elevated temperature and CO2 increased root dry weights of the radishes ‘Cheongdae and Chunha’ more than elevated temperature alone. When the cabbage ‘Chun-gwang’ was grown for 90 DAS with the elevated CO2 concentration, the leaf dry weight was about 3-fold higher than that of the same cultivar grown in ambient CO2 concentration conditions (Fig. 2). However, when ‘Chun-gwang’ was exposed to both elevated CO2 and elevated temperature for 90 DAS, the leaf dry weight was approximately 3-fold lower than that of plants grown with the elevated CO2 alone. In contrast, when the cabbage ‘Jincheong’ was grown in elevated CO2, the leaf dry weight was less than that from plants that were grown with the ambient CO2 concentration, regardless of the temperature. The leaf dry weight of the cabbage ‘Jincheong’ decreased by 36 ± 5% at 90 DAS under elevated temperature, compared with those that were grown in ambient temperature. When the cabbage ‘Samjin’ was grown under either elevated temperature alone or both elevated temperature and CO2 for 80 DAS, the decrease in the leaf dry weight was less than that of the other cabbage cultivars. The elevated temperature decreased the root to shoot ratio in the radish ‘Chun-ha; however, the decrease in the ratio was less than the radish ‘Cheong-dae’. Also this ratio did not decrease when ‘Chunha’ was exposed to a combination of elevated CO2 and temperature, compared with those that were exposed to elevated temperature alone (Fig. 3). The root to shoot ratio in the radishes ‘Cheongdae and Cheong-un’ decreased when they were exposed to either elevated temperature alone or both elevated temperature and CO2 for 90 DAS. The elevated CO2 increased the root to shoot ratio in the cabbage ‘Chun-gwang’ about 2-fold only at the seedling stage, 8 DAS, than that was grown in ambient CO2 (Fig. 4). A combination of elevated temperature and CO2 significantly increased this ratio in the cabbages ‘Jincheong’ and ‘Samjin’ than those exposed to elevated temperature alone at the seedling or young plant stage, 8 DAS and 25 DAS, respectively.

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When the radish ‘Cheongdae’ was exposed to the elevated temperature for 90 DAS, the root length and diameter decreased by 56 ± 5% and 63 ± 1%, respectively (Table 1). Moreover, the decrease in its root diameter was significant when it was exposed to both elevated temperature and CO2 than when it was exposed to the elevated temperature alone. While both of the root diameter and length of the radishes ‘Chunha’ and ‘Cheong-un’ grown at the elevated temperature were lower than those grown at the ambient temperature. The decrease in the root diameter was greater than that in the root length.

Fig. 2. Leaf dry weights of the cabbages ‘Chun-gwang’ and -1 ‘Jincheong’ exposed to either ambient CO2 (350 µmolmol ) or -1 elevated CO2 (650 µmolmol ) in both ambient and elevated temperature (ambient + 4°C) for 45 and 90 DAS and ‘Samjin’ at 60 and 80 DAS. Bars represent the mean dry weight for 3 plants ± standard error.


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Fig. 3. Root to shoot dry weight ratios of the radishes ‘Cheongdae’ -1 and ‘Chunha’ exposed to either ambient CO2 (350 µmolmol ) -1 or elevated CO2 (650 µmolmol ) in both ambient and elevated temperature (ambient + 4°C) for 8, 20, 45 and 90 DAS and ‘Cheong-un’ for 25, 60, and 80 DAS. Bars represent the mean dry weight for 3 plants ± standard error.

Fig. 4. Root to shoot dry weight ratios of the cabbages ‘Chun-gwang’ -1 and ‘Jincheong’exposed to either ambient CO2 (350 µmolmol ) -1 or elevated CO2 (650 µmolmol ) in both ambient and elevated temperature (ambient + 4°C) for 8, 20, 45 and 90 DAS and ‘Samjin’ for 25, 60, and 80 DAS. Bars represent the mean dry weight for 3 plants ± standard error.

Table 1. Root length and diameter of the radishes exposed to either ambient CO2 (350 µmolmol-1) or elevated CO2 (650 µmolmol-1) in both ambient and elevated temperature (ambient + 4°C) for 90 days after sowing (DAS). Ambient temperature Cultivar

Ambient CO2

Elevated temperature

Elevated CO2

Ambient CO2

Elevated CO2

Root length (cm)z ‘Cheongdae’

1

18.4(1.8)

17.0(1.2)

8.2(0.2)

10.3(0.9)

‘Chunha’

25.7(1.2)

23.1(1.7)

22.5(0.8)

21.0(2.0)

‘Cheong-un’

23.3(0.9)

23.0(1.7)

22.2(1.0)

24.0(0.6)

y

Root diameter (mm)

z

‘Cheongdae’

85.5(6.5)

77.7(6.3)

34.9(2.0)

50.3(0.3)

‘Chunha’

76.2(2.0)

70.0(3.8)

62.0(2.1)

70.0(2.5)

‘Cheong-un’

79.5(3.9)

74.7(5.4)

64.0(2.3)

61.0(1.5)

Main axis length of root was measured manually. The level of thickest part of radish was measured manually. Data were presented with means of 3 replications with standard error. y


Udwh# ri# Skrwrv|qwkhvlv# dqg# Jdv# H{fkdqjh When the radishes were exposed to elevated CO2 in long-term period, increases in stomatal conductance, transpiration rate, internal CO2 concentration were observed in ‘Cheongdae’ and ‘Chunha’, whereas decrease were observed in ‘Cheong-un’, compared with those that were grown in the ambient CO2 concentration (Table 2). However, the long-term exposure to elevated CO2 did not influence greatly on their rates of photosynthesis. While the elevated temperature increased the rate of photosynthesis of the radish ‘Chunha’, it did not have any effect on that of the radishes ‘Cheongdae’ and ‘Cheong-un’, compared with those that were grown in the ambient CO2 condition. For all 3 cultivars of cabbage, the elevated CO2 concentration slightly decreased the stomatal conductance (Table 3); however, it only had a negligible effect on the internal CO2 concentrations. Only the rate of photosynthesis in the cabbage ‘Chung-gwang’ was lower when they were exposed to the elevated CO2 concentration for long periods. The cabbages ‘Chun-gwang’ and ‘Samjin’ exhibited slightly lower rates of photosynthesis when they were grown at the elevated temperature than those grown at the ambient temperature. However, the decrease in the

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photosynthesis rate of the cabbage ‘Chun-gwang’ exposed to both elevated temperature and CO2 was more significant than that in the other cabbage cultivars. In addition, the stomatal conductance and internal CO2 concentration of the ‘Chun-gwang’ decreased by about 83% and 23%, respectively, under both elevated temperature and CO2 than those grown under control condition. Udwh# ri# Qxwulhqw# Xswdnh The levels of nutrients that were absorbed by the radish cultivars grown in different conditions were compared. The roots of all 3 radish cultivars accumulated more potassium (K) than in the leaves, whereas the leaves accumulated more calcium (Ca) than the roots (Fig. 5). The concentration of K in the roots of the radishes ‘Cheongdae’ and ‘Cheong-un’ was higher when the plants were grown at the elevated temperature for long periods than when grown in other conditions. Although there was no difference in the concentration of K in the roots of the radish ‘Cheong-un’ in any condition, the highest concentration of Ca occurred in its leaves. When the rates of nutrient uptake by these plants were calculated by using Williams’ (1948) formula, the rates of uptake for

Table 2. Photosynthesis [µmol CO2 m-2s-1], transpiration rate [mol H2O m-2s-1], water vapor saturation deficit at leaf surface [VpdL: -2 -1 -2 -1 -1 mol H2O m s ], stomatal conductance [mol H2O m s ], internal CO2 [µmol CO2 mol air] of fully expanded radish leaves exposed -1 -1 to either ambient CO2 (350 µmolmol ) or elevated CO2 (650 µmolmol ) in both ambient and elevated temperature (ambient + 4°C). Ambient temperature


Ambient CO2

Elevated CO2

Ambient CO2

Elevated CO2

Photosynthesis

24.7(0.5)

22.8(0.6)

24.6(0.9)

23.0(0.2)

Transpiration rate

6.8(0.02)

8.9(0.2)

9.8(0.4)

8.9(0.1)

1.5(0.1)

1.2(0.1)

1.0(0.04)

1.1(0.02)

Conductance

0.5(0.05)

1.1(0.16)

1.5(0.17)

1.1(0.01)

Internal CO2

268(6)

312(4)

319(1)

317(1)

Photosynthesis

24.9(0.4)

24.0(0.06)

27.6(0.4)

24.2(0.3)

Transpiration rate

7.2(0.06)

9.5(0.2)

10.7(0.5)

9.1(0.07)

VpdL

1.4(0.07)

1.0(0.01)

0.8(0.06)

1.1(0.04)

Conductance

0.6(0.03)

1.3(0.03)

3.2(0.7)

1.2(0.08)

Internal CO2

280(3)

318(0.4)

324(3)

314(2)

19.8(0.4)

17.1(0.5)

18.7(0.6)

18.2(0.2)

Transpiration rate

3.54(0.05)

2.45(0.09)

2.34(0.07)

2.68(0.04)

VpdL

0.74(0.01)

0.92(0.02)

0.95(0.02)

0.90(0.04)

Conductance

0.58(0.02)

0.30(0.02)

0.27(0.01)

0.34(0.01)

Internal CO2

306(3)

272(3)

243(4)

276(7)

Radish ‘Cheongdae’

VpdL

Radish ‘Chunha’

Radish ‘Cheong-un’ Photosynthesis

Data were represented with means of 6 replications and standard error of the replications. Each observation was repeated 4 times on three leaves randomly selected from 3 individual plants of each cultivar, and this observation was repeated 2 times at 70 and 75 DAS.

382


total nitrogen (T-N), phosphorus (P), and K in the control condition were higher in the radish ‘Cheongdae’ than in the ‘Chunha and Cheong-un’ (Fig. 6). However, either the elevated temperature alone or both elevated temperature and CO2 increased the rates of uptake of T-N, P, K, and Ca in the radish ‘Chunha’. In particular, its rates of uptake of T-N, P, K, and Ca in the elevated temperature condition were 7.9, 1.7, 1.9, and 2.9 times greater, respectively, than those of ‘Cheongdae.’ In addition, its rates of uptake of T-N, P, K, and Ca in a combination of elevated CO2 and temperature condition were 3.6, 4.3, 1.5, and 11.9 times greater, respectively, than those of ‘Cheongdae.’

those grown in ambient CO2 (Fig. 2). Many previous studies have shown that long-term exposure to CO2 inhibits plant growth (Cave et al., 1981; DeLucia et al., 1985; Sasek et al., 1985; von Caemmerer et al., 1984; Wong, 1979). One possible reason for this effect is the feedback inhibition as a result of excessive carbohydrate loading of leaves by enlarged starch grains, which physically damages chloroplasts (reviewed by Sage et al., 1989 and references therein; Sasek et al., 1985). However, a significant increase in leaf starch content with no growth inhibition was observed when all of the tested plants in this study were exposed to the long-term elevated CO2, except for the cabbage ‘Jincheong’ (unpublished data). This result indicated that increased starch content in the leaves under the long-term elevated CO2 condition is not a crucial cause that inhibits plant growth. In the cabbage ‘Chun-gwang’, elevated CO2 decreased the rate of photosynthesis, stomatal conductance and internal CO2 concentration, although the elevated CO2 greatly increased the leaf dry weight (Table 3). This result may be due that the measurement of photosynthesis rate was carried during far later period than during the plant growth and development. Otherwise, decrease in photosynthesis at elevated CO2 concentrations is known

Glvfxvvlrq Our results showed that the plant growth, rate of photosynthesis, gas exchange, and rate of nutrient uptake in these conditions differed between the radish and cabbage as well as between their cultivars. Long-term elevated CO2 more greatly influenced to the cabbage; but not the radish. The cabbage ‘Chun-gwang’ exposed to the elevated CO2 for 90 DAS greatly increased the leaf dry weight, whereas the cabbage ‘Jincheong’ decreased the leaf dry weight, compared to

Table 3. Photosynthesis [µmol CO2 m-2s-1], transpiration rate [mol H2O m-2s-1], water vapor saturation deficit at leaf surface [VpdL: -2 -1 -2 -1 -1 mol H2O m s ], stomatal conductance [mol H2O m s ], internal CO2 [µmol CO2 mol air] of fully expanded cabbage leaves exposed -1 -1 to either ambient CO2 (350 µmolmol ) or elevated CO2 (650 µmolmol ) in both ambient and elevated temperature (ambient + 4°C). Ambient temperature


Elevated CO2

Ambient CO2

Elevated CO2

21.9(0.3)

15.6(0.2)

18.2(0.1)

11.2(1.0)

7.5(0.2)

6.0(0.08)

8.7(0.3)

3.4(0.2)

VpdL

1.3(0.02)

1.9(0.07)

1.3(0.02)

2.6(0.09)

Conductance

0.7(0.01)

0.3(0.01)

0.8(0.02)

0.1(0.01)

Internal CO2

302(1)

286(2)

321(1)

230(3)

17.3(0.5)

17.4(0.7)

17.2(0.4)

17.6(0.2)

Ambient CO2 Cabbage‘Chun-gwang’ Photosynthesis Transpiration rate

Cabbage ‘Jincheong’ Photosynthesis Transpiration rate

7.1(0.2)

6.9(0.3)

7.1(0.3)

8.0(0.08)

VpdL

1.4(0.1)

1.7(0.01)

1.6(0.1)

1.5(0.01)

Conductance

0.6(0.07)

0.5(0.02)

0.6(0.07)

0.6(0.01)

Internal CO2

320(4)

295(1)

303(4)

313(0.6)

14.5(0.4)

13.4(0.6)

12.8(0.4)

12.7(0.3)

Transpiration rate

3.10(0.01)

2.80(0.09)

2.50(0.05)

2.50(0.04)

VpdL

0.81(0.01)

0.90(0.01)

0.96(0.02)

0.84(0.02)

Conductance

0.44(0.01)

0.35(0.01)

0.31(0.01)

0.34(0.01)

Internal CO2

313(2)

310(2)

299(1)

313(1)

Cabbage ‘Samjin’ Photosynthesis

Data were represented with means of 6 replications and standard error of the replications. Each observation was repeated 4 times on three leaves randomly selected from 3 individual plants of each cultivar, and this observation was repeated 2 times at 70 and 75 DAS.


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Fig. 5. Concentrations of mineral nutrients in the leaves and roots of the radishes ‘Cheongdae’ and ‘Chunha’ exposed to either ambient -1 -1 CO2 (350 µmolmol ) or elevated CO2 (650 µmolmol ) in both ambient and elevated temperature (ambient + 4°C) for 90 DAS and ‘Cheong-un’ for 80 DAS. Bars represent the mean dry weight for 4 plants ± standard error.

to be associated with a decreased demand for carbohydrates, as a result of the accumulation of starch and sucrose in this condition as hypothesized in previous studies (DeLucia et al., 1985; Ehret and Joliffe, 1985). In addition, the decrease in the stomatal conductance and internal CO2 concentration was found in the 3 cabbage cultivars during long-term exposure to elevated CO2, while the opposite result was found in the radish cultivars ‘Cheongdae’ and ‘Chunha’. It may be associated

with cabbage’s relatively smaller sink capacity than that of radish plant for excess carbohydrates in leaves. On the other hand, radish has a large sink capacity in its roots, which affects the photosynthesis activity of its leaves (Usuda and Shimogawara, 1998). Further research on direct cause of growth inhibition under the long-term elevated CO2 and its variable effects depending on cultivars or species is necessary to conduct. As a result of acclimating to the elevated temperature,

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Fig. 6. Uptake rates of nutrient by the roots of radishes ‘Cheongdae’ and ‘Chunha’ for 45 days between 45 and 90 DAS, and by the -1 root of radish ‘Cheong-un’ for 20 days between 60 and 80 DAS. Plants were exposed to either ambient CO2 (350 µmolmol ) or -1 elevated CO2 (650 µmolmol ) in both ambient and elevated temperature (ambient + 4°C). Bars represent the mean dry weight for 4 plants ± standard error.

the radish ‘Chunha’ had a higher rate of photosynthesis, stomatal conductance, and internal CO2 concentration than in the control condition (Table 2). Previous studies have hypothesized that the photosynthetic apparatus can acclimate to new temperature regimes by increasing the rate of photosynthesis (Bradshaw and Holzapfel, 2006; van Dijk and Hautekeete, 2007). In current study, long-term exposure to both elevated temperature and CO2 increased the root dry weight of the radish ‘Chunha’ more than the elevated temperature alone (Figs. 1, 3, and Table 1). Also, a combination of elevated temperature and CO2 significantly increased this ratio in the cabbages ‘Jincheong and Samjin’ than those exposed to elevated temperature alone at the seedling or young plant stage, 8 DAS and 25 DAS, respectively (Fig. 4). These results suggested that an increase in CO2 concentration when the plants are exposed to elevated temperatures for long periods might offset the decrease in photosynthesis due to increased photorespiration at elevated temperatures. As a result, the radish ‘Chunha’ may be able to develop photosynthetic thermotolerance by modulating its stomatal conductance in response to long-term exposure to both elevated temperature and CO2. Although the specific mechanisms of the effect of elevated temperature on net photosynthesis are unclear (Crafts-Brandner and Salvucci, 2004; Schrader et al., 2004),

it is clear that photorespiration is one reason that photosynthetic efficiency decreases at elevated temperatures (Sage and Sharkey, 1987). In addition, this acclimation may be related to a higher rate of nutrient uptake when either temperature alone or both temperature and CO2 concentration is elevated, as in the radish ‘Chunha’ (Fig. 6). The root to shoot ratio is an important indicator of root growth that is necessary for the uptake and allocation of nutrients and photosynthates (Rogers et al., 1996). The combination of elevated CO2 and temperature stimulated the growth of roots more than that of shoots in the radish ‘Chunha’, which may have increased the rate of nutrient uptake (Fig. 6). The decrease in the rate of photosynthesis and dry weight of the roots of the cabbage ‘Chun-gwang’ at a combination condition of elevated temperature and CO2 was greater than other cabbage cultivars (Table 3 and Fig. 2). Furthermore, the internal CO2 concentration, stomatal conductance, and rate of photosynthesis decreased significantly while the VpdL increased significantly. The significant decrease in stomatal conductance might cause a decrease in the internal CO2 concentration, which could increase the heat stress in leaves (Table 3). The increased VpdL could reduce the stomatal conductance, which would reduce the intercellular CO2 concentration and photosynthesis (Berry and Bjorkman 1980; Fredeen and Sage, 1999). Wang


et al. (2008) showed that acute heat stress in cool-season (C3) species increased the stomatal limitations to photosynthesis and concluded that the positive effects of elevated CO2 on photosynthesis at ambient temperatures may be partly offset by the negative effects of acute heat stress, especially for C4 species. In this study, we could not prove a cause and effect relationship between the decrease in growth and stomatal conductance due to elevated CO2 level and temperature. Therefore, we propose the following hypothesis to explain our observations. We propose that the tolerance to either elevated temperature alone or a combination condition of elevated CO2 and temperature is associated with an increase in stomatal conductance and intercellular CO2 to compensate for reduced photosynthesis due to photorespiration. Since increased stomatal conductance and decreased VpdL in unfavorable climate conditions seem to be correlated with tolerance to elevated CO2 and temperature, these parameters may be good indicators of the tolerance to these stresses. In conclusion, an analysis of the dry weight, rate of photosynthesis, or rate of nutrient uptake indicated that the radish ‘Chunha’ and the cabbage ‘Samjin’ tolerated either elevated temperature alone or both elevated temperature and CO2. Acknowledgements: This study was conducted with a financial support of the National Institute of Horticulture and Herbal Science for the first author, who worked as a postdoctoral fellow in the Institute.

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